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Review

Role of interferon in melanoma: old hopes and new perspectives

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Pages 475-483 | Received 30 Aug 2016, Accepted 27 Jan 2017, Published online: 16 Feb 2017

References

  • Isaacs A, Lindenmann J. Virus interference. I. The interferon. Proc R Soc Lond B Biol Sci. 1957;147:258–267.
  • Lindenmann J. Induction of chick interferon: procedures of the original experiments. Methods Enzymol. 1981;78:181–188.
  • Pestka S, Langer JA, Zoon KC, et al. Interferons and their actions. Annu Rev Biochem. 1987;56:727–777.
  • Pestka S. Interferon standards and general abbreviations. Methods Enzymol. 1986;119:14–23.
  • Kotenko SV, Gallagher G, Baurin VV, et al. IFN-lambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat Immunol. 2003;4:69–77.
  • Darnell JE, Kerr IM, Stark GR. Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science. 1994;264:1415–1421.
  • Ihle JN. The Janus protein tyrosine kinase family and its role in cytokine signaling. Adv Immunol. 1995;60:1–35.
  • Bach EA, Aguet M, Schreiber RD. The IFN gamma receptor: a paradigm for cytokine receptor signaling. Annu Rev Immunol. 1997;15:563–591.
  • Chen J, Baig E, Fish EN. Diversity and relatedness among the type I interferons. J Interferon Cytokine Res Off J Int Soc Interferon Cytokine Res. 2004;24:687–698.
  • Platanias LC. The p38 mitogen-activated protein kinase pathway and its role in interferon signaling. Pharmacol Ther. 2003;98:129–142.
  • Rafique I, Kirkwood JM, Tarhini AA. Immune checkpoint blockade and interferon-α in melanoma. Semin Oncol. 2015;42:436–447.
  • Dunn GP, Koebel CM, Schreiber RD. Interferons, immunity and cancer immunoediting. Nat Rev Immunol. 2006;6:836–848.
  • Zhou Z, Hamming OJ, Ank N, et al. Type III interferon (IFN) induces a type I IFN-like response in a restricted subset of cells through signaling pathways involving both the Jak-STAT pathway and the mitogen-activated protein kinases. J Virol. 2007;81:7749–7758.
  • Vilcek J. Novel interferons. Nat Immunol. 2003;4:8–9.
  • Miller CHT, Maher SG, Young HA. Clinical use of interferon-gamma. Ann N Y Acad Sci. 2009;1182:69–79.
  • Platanias LC. Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat Rev Immunol. 2005;5:375–386.
  • Krasagakis K, Garbe C, Krüger S, et al. Effects of interferons on cultured human melanocytes in vitro: interferon-beta but not-alpha or -gamma inhibit proliferation and all interferons significantly modulate the cell phenotype. J Invest Dermatol. 1991;97:364–372.
  • Roh MR, Zheng Z, Kim HS, et al. Difference of interferon-α and interferon-β on melanoma growth and lymph node metastasis in mice. Melanoma Res. 2013;23:114–124.
  • Kubo H, Ashida A, Matsumoto K, et al. Interferon-beta therapy for malignant melanoma: the dose is crucial for inhibition of proliferation and induction of apoptosis of melanoma cells. Arch Dermatol Res. 2008;300:297–301.
  • Horikoshi T, Fukuzawa K, Hanada N, et al. In vitro comparative study of the antitumor effects of human interferon-alpha, beta and gamma on the growth and invasive potential of human melanoma cells. J Dermatol. 1995;22:631–636.
  • Raig ET, Jones NB, Varker KA, et al. VEGF secretion is inhibited by interferon-alpha in several melanoma cell lines. J Interferon Cytokine Res Off J Int Soc Interferon Cytokine Res. 2008;28:553–561.
  • Bölling B, Fandrey J, Frosch PJ, et al. VEGF production, cell proliferation and apoptosis of human IGR 1 melanoma cells under nIFN-alpha/beta and rIFN-gamma treatment. Exp Dermatol. 2000;9:327–335.
  • McMillan TJ, Rao J, Everett CA, et al. Interferon-induced alterations in metastatic capacity, class-1 antigen expression and natural killer cell sensitivity of melanoma cells. Int J Cancer J Int Cancer. 1987;40:659–663.
  • Basham TY, Bourgeade MF, Creasey AA, et al. Interferon increases HLA synthesis in melanoma cells: interferon-resistant and -sensitive cell lines. Proc Natl Acad Sci U S A. 1982;79:3265–3269.
  • Giacomini P, Fraioli R, Calabrò AM, et al. Class I major histocompatibility complex enhancement by recombinant leukocyte interferon in the peripheral blood mononuclear cells and plasma of melanoma patients. Cancer Res. 1991;51:652–656.
  • Heise R, Amann PM, Ensslen S, et al. Interferon alpha signalling and its relevance for the upregulatory effect of transporter proteins associated with antigen processing (TAP) in patients with malignant melanoma. slominski AT editor. Plos One. 2016;11:e0146325.
  • Losinno C, Wines BD, Johns TG, et al. Natural killer cell activity against cultured melanoma cells: a dye-reduction technique with studies on augmented activity by interferon subtypes. Nat Immun. 1992;11:215–224.
  • Palmer KJ, Harries M, Gore ME, et al. Interferon-alpha (IFN-alpha) stimulates anti-melanoma cytotoxic T lymphocyte (CTL) generation in mixed lymphocyte tumour cultures (MLTC). Clin Exp Immunol. 2000;119:412–418.
  • Lesinski GB, Anghelina M, Zimmerer J, et al. The antitumor effects of IFN-α are abrogated in a STAT1-deficient mouse. J Clin Invest. 2003;112:170–180.
  • Kolumam GA, Thomas S, Thompson LJ, et al. Type I interferons act directly on CD8 T cells to allow clonal expansion and memory formation in response to viral infection. J Exp Med. 2005;202:637–650.
  • Kirkwood JM, Richards T, Zarour HM, et al. Immunomodulatory effects of high-dose and low-dose interferon alpha2b in patients with high-risk resected melanoma: the E2690 laboratory corollary of intergroup adjuvant trial E1690. Cancer. 2002;95:1101–1112.
  • Paquette RL, Hsu NC, Kiertscher SM, et al. Interferon-alpha and granulocyte-macrophage colony-stimulating factor differentiate peripheral blood monocytes into potent antigen-presenting cells. J Leukoc Biol. 1998;64:358–367.
  • Brinkmann V, Geiger T, Alkan S, et al. Interferon alpha increases the frequency of interferon gamma-producing human CD4+ T cells. J Exp Med. 1993;178:1655–1663.
  • Wenner CA, Güler ML, Macatonia SE, et al. Roles of IFN-gamma and IFN-alpha in IL-12-induced T helper cell-1 development. J Immunol Baltim Md. 1950/1996;156:1442–1447.
  • Håkansson A, Gustafsson B, Krysander L, et al. Effect of IFN-alpha on tumor-infiltrating mononuclear cells and regressive changes in metastatic malignant melanoma. J Interferon Cytokine Res Off J Int Soc Interferon Cytokine Res. 1998;18:33–39.
  • Håkansson A, Gustafsson B, Krysander L, et al. Effect of interferon-alpha on the expression of tumour necrosis factor-alpha by metastatic malignant melanoma in vivo. Melanoma Res. 1997;7:139–145.
  • Ismail A, Yusuf N. Type I interferons: key players in normal skin and select cutaneous malignancies. Dermatol Res Pract. 2014;2014:847545.
  • Moschos SJ, Edington HD, Land SR, et al. Neoadjuvant treatment of regional stage IIIB melanoma with high-dose interferon alfa-2b induces objective tumor regression in association with modulation of tumor infiltrating host cellular immune responses. J Clin Oncol Off J Am Soc Clin Oncol. 2006;24:3164–3171.
  • Di Pucchio T, Pilla L, Capone I, et al. Immunization of stage IV melanoma patients with Melan-A/MART-1 and gp100 peptides plus IFN-alpha results in the activation of specific CD8(+) T cells and monocyte/dendritic cell precursors. Cancer Res. 2006;66:4943–4951.
  • Tsavaris N, Baxevanis C, Kosmidis P, et al. The prognostic significance of immune changes in patients with renal cancer, melanoma and colorectal cancer, treated with interferon alpha 2b. Cancer Immunol Immunother CII. 1996;43:94–102.
  • Tarhini AA, Kirkwood JM. Clinical and immunologic basis of interferon therapy in melanoma. Ann N Y Acad Sci. 2009;1182:47–57.
  • Kirkwood JM, Strawderman MH, Ernstoff MS, et al. Interferon alfa-2b adjuvant therapy of high-risk resected cutaneous melanoma: the Eastern Cooperative Oncology Group Trial EST 1684. J Clin Oncol Off J Am Soc Clin Oncol. 1996;14:7–17.
  • Kirkwood JM, Ibrahim JG, Sondak VK, et al. High- and low-dose interferon alfa-2b in high-risk melanoma: first analysis of intergroup trial E1690/S9111/C9190. J Clin Oncol Off J Am Soc Clin Oncol. 2000;18:2444–2458.
  • Kirkwood JM, Ibrahim J, Lawson DH, et al. High-dose interferon alfa-2b does not diminish antibody response to GM2 vaccination in patients with resected melanoma: results of the multicenter eastern cooperative oncology group phase II trial E2696. J Clin Oncol Off J Am Soc Clin Oncol. 2001;19:1430–1436.
  • Kirkwood JM, Ibrahim JG, Sosman JA, et al. High-dose interferon alfa-2b significantly prolongs relapse-free and overall survival compared with the GM2-KLH/QS-21 vaccine in patients with resected stage IIB-III melanoma: results of intergroup trial E1694/S9512/C509801. J Clin Oncol Off J Am Soc Clin Oncol. 2001;19:2370–2380.
  • Garbe C, Radny P, Linse R, et al. Adjuvant low-dose interferon {alpha}2a with or without dacarbazine compared with surgery alone: a prospective-randomized phase III DeCOG trial in melanoma patients with regional lymph node metastasis. Ann Oncol Off J Eur Soc Med Oncol ESMO. 2008;19:1195–1201.
  • Payne MJ, Argyropoulou K, Lorigan P, et al. Phase II pilot study of intravenous high-dose Interferon with or without maintenance treatment in melanoma at high risk of recurrence. J Clin Oncol Off J Am Soc Clin Oncol. 2014;32:185–190.
  • Eggermont AMM, Suciu S, Rutkowski P, et al. Long term follow up of the EORTC 18952 trial of adjuvant therapy in resected stage IIB–III cutaneous melanoma patients comparing intermediate doses of interferon-alpha-2b (IFN) with observation: ulceration of primary is key determinant for IFN-sensitivity. Eur J Cancer. 2016;55:111–121.
  • Mocellin S, Pasquali S, Rossi CR, et al. Interferon alpha adjuvant therapy in patients with high-risk melanoma: a systematic review and meta-analysis. J Natl Cancer Inst. 2010;102:493–501.
  • Wheatley K, Ives N, Hancock B, et al. Does adjuvant interferon-alpha for high-risk melanoma provide a worthwhile benefit? A meta-analysis of the randomised trials. Cancer Treat Rev. 2003;29:241–252.
  • Eggermont AMM, Suciu S, Testori A, et al. Ulceration and stage are predictive of interferon efficacy in melanoma: results of the phase III adjuvant trials EORTC 18952 and EORTC 18991. Eur J Cancer Oxf Engl. 1990/2012;48:218–225.
  • Eggermont AMM, Suciu S, Testori A, et al. Long-term results of the randomized phase III trial EORTC 18991 of adjuvant therapy with pegylated interferon alfa-2b versus observation in resected stage III melanoma. J Clin Oncol Off J Am Soc Clin Oncol. 2012;30:3810–3818.
  • Grob JJ, Jouary T, Dréno B, et al. Adjuvant therapy with pegylated interferon alfa-2b (36 months) versus low-dose interferon alfa-2b (18 months) in melanoma patients without macrometastatic nodes: an open-label, randomised, phase 3 European association for dermato-oncology (EADO) study. Eur J Cancer Oxf Engl. 1990/2013;49:166–174.
  • Wang W, Edington HD, Rao UNM, et al. Modulation of signal transducers and activators of transcription 1 and 3 signaling in melanoma by high-dose IFNalpha2b. Clin Cancer Res Off J Am Assoc Cancer Res. 2007;13:1523–1531.
  • Hofmann MA, Kiecker F, Küchler I, et al. Serum TNF-α, B2M and sIL-2R levels are biological correlates of outcome in adjuvant IFN-α2b treatment of patients with melanoma. J Cancer Res Clin Oncol. 2011;137:455–462.
  • Simons DL, Lee G, Kirkwood JM, et al. Interferon signaling patterns in peripheral blood lymphocytes may predict clinical outcome after high-dose interferon therapy in melanoma patients. J Transl Med. 2011;9:52.
  • Håkansson A, Gustafsson B, Krysander L, et al. Tumour-infiltrating lymphocytes in metastatic malignant melanoma and response to interferon alpha treatment. Br J Cancer. 1996;74:670–676.
  • Sasse AD, Sasse EC, Clark LGO, et al. Chemoimmunotherapy versus chemotherapy for metastatic malignant melanoma. Cochrane Database Syst Rev. 2007;(1):CD005413.
  • Ives NJ, Stowe RL, Lorigan P, et al. Chemotherapy compared with biochemotherapy for the treatment of metastatic melanoma: a meta-analysis of 18 trials involving 2,621 patients. J Clin Oncol Off J Am Soc Clin Oncol. 2007;25:5426–5434.
  • Xin Y, Huang Q, Zhang P, et al. Meta-analysis of the safety and efficacy of interferon combined with dacarbazine versus dacarbazine alone in cutaneous malignant melanoma. Medicine (Baltimore). 2016;95:e3406.
  • Brunet JF, Denizot F, Luciani MF, et al. A new member of the immunoglobulin superfamily–CTLA-4. Nature. 1987;328:267–270.
  • Waterhouse P, Penninger JM, Timms E, et al. Lymphoproliferative disorders with early lethality in mice deficient in Ctla-4. Science. 1995;270:985–988.
  • Hanson DC, Canniff PC, Primiano MJ, et al. Preclinical in vitro characterization of anti-CTLA4 therapeutic antibody CP-675,206. Cancer Res. 2004;64:877–877.
  • Ribas A, Comin-Anduix B, Economou JS, et al. Intratumoral immune cell infiltrates, FoxP3, and indoleamine 2,3-dioxygenase in patients with melanoma undergoing CTLA4 blockade. Clin Cancer Res Off J Am Assoc Cancer Res. 2009;15:390–399.
  • Tarhini AA, Cherian J, Moschos SJ, et al. Safety and efficacy of combination immunotherapy with interferon alfa-2b and tremelimumab in patients with stage IV melanoma. J Clin Oncol Off J Am Soc Clin Oncol. 2012;30:322–328.
  • Home - ClinicalTrials.gov [Internet]. [cited 2013 Sep 18]. Available from: http://clinicaltrials.gov/.
  • Zou W, Wolchok JD, Chen L. PD-L1 (B7-H1) and PD-1 pathway blockade for cancer therapy: mechanisms, response biomarkers, and combinations. Sci Transl Med. 2016;8:328rv4.
  • Topalian SL, Taube JM, Anders RA, et al. Mechanism-driven biomarkers to guide immune checkpoint blockade in cancer therapy. Nat Rev Cancer. 2016;16:275–287.
  • Gerner MY, Heltemes-Harris LM, Fife BT, et al. Cutting edge: IL-12 and type I IFN differentially program CD8 T cells for programmed death 1 re-expression levels and tumor control. J Immunol Baltim Md. 1950/2013;191:1011–1015.
  • Mühlbauer M, Fleck M, Schütz C, et al. PD-L1 is induced in hepatocytes by viral infection and by interferon-alpha and -gamma and mediates T cell apoptosis. J Hepatol. 2006;45:520–528.
  • Gowrishankar K, Gunatilake D, Gallagher SJ, et al. Inducible but not constitutive expression of PD-L1 in human melanoma cells is dependent on activation of NF-κB. Plos ONE [Internet]. 2015; 10: cited 2016 May 8]. Available from http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4386825/
  • Zarour HM, Tawbi H, Tarhini AA, et al. Study of anti-PD-1 antibody pembrolizumab and pegylated-interferon alfa-2b (Peg-IFN) for advanced melanoma. J Clin Oncol [Internet]. 2015;33(suppl; abstr e20018):cited 2016 May 9. Available from http://meetinglibrary.asco.org/content/152481-156
  • Kumar KGS, Liu J, Li Y, et al. Raf inhibitor stabilizes receptor for the type I interferon but inhibits its anti-proliferative effects in human malignant melanoma cells. Cancer Biol Ther. 2007;6:1437–1441.
  • Frederick DT, Piris A, Cogdill AP, et al. BRAF inhibition is associated with enhanced melanoma antigen expression and a more favorable tumor microenvironment in patients with metastatic melanoma. Clin Cancer Res Off J Am Assoc Cancer Res. 2013;19:1225–1231.
  • Sapkota B, Hill CE, Pollack BP. Vemurafenib enhances MHC induction in BRAF(V600E) homozygous melanoma cells. Oncoimmunology. 2013;2:e22890.
  • Ascierto PA, Grimaldi AM, Acquavella N, et al. Future perspectives in melanoma research. meeting report from the “Melanoma Bridge. Napoli, December 2nd-4th 2012. J Transl Med. 2013;11:137.
  • Ferrari De AL, Ngiow SF, Stannard K, et al. Natural killer cells are essential for the ability of BRAF inhibitors to control BRAFV600E-mutant metastatic melanoma. Cancer Res. 2014;74:7298–7308.
  • Sanlorenzo M, Vujic I, Moy A, et al. Synergy of molecular targeted approaches and immunotherapy in melanoma: preclinical basis and clinical perspectives. Expert Opin Biol Ther. 2015;15:1491–1500.
  • Parker BS, Rautela J, Hertzog PJ. Antitumour actions of interferons: implications for cancer therapy. Nat Rev Cancer. 2016;16:131–144.
  • Fuchs SY. Hope and fear for interferon: the receptor-centric outlook on the future of interferon therapy. J Interferon Cytokine Res Off J Int Soc Interferon Cytokine Res. 2013;33:211–225.
  • Zheng H, Qian J, Varghese B, et al. Ligand-stimulated downregulation of the alpha interferon receptor: role of protein kinase D2. Mol Cell Biol. 2011;31:710–720.
  • Zheng H, Qian J, Carbone CJ, et al. Vascular endothelial growth factor-induced elimination of the type 1 interferon receptor is required for efficient angiogenesis. Blood. 2011;118:4003–4006.
  • Huangfu W-C, Qian J, Liu C, et al. Inflammatory signaling compromises cell responses to interferon alpha. Oncogene. 2012;31:161–172.
  • Bhattacharya S, HuangFu W-C, Dong G, et al. Anti-tumorigenic effects of Type 1 interferon are subdued by integrated stress responses. Oncogene. 2013;32:4214–4221.
  • Song MM, Shuai K. The suppressor of cytokine signaling (SOCS) 1 and SOCS3 but not SOCS2 proteins inhibit interferon-mediated antiviral and antiproliferative activities. J Biol Chem. 1998;273:35056–35062.
  • Porritt RA, Hertzog PJ. Dynamic control of type I IFN signalling by an integrated network of negative regulators. Trends Immunol. 2015;36:150–160.
  • Pan M, Kalie E, Scaglione BJ, et al. Mutation of the IFNAR-1 receptor binding site of human IFN-alpha2 generates type I IFN competitive antagonists. Biochemistry (Mosc.). 2008;47:12018–12027.
  • Eggermont AMM, Suciu S, Santinami M, et al. Adjuvant therapy with pegylated interferon alfa-2b versus observation alone in resected stage III melanoma: final results of EORTC 18991, a randomised phase III trial. Lancet Lond Engl. 2008;372:117–126.
  • Aranda F, Vacchelli E, Obrist F, et al. Trial Watch: toll-like receptor agonists in oncological indications. Oncoimmunology. 2014;3:e29179.
  • Qin M, Li Y, Yang X, et al. Safety of Toll-like receptor 9 agonists: a systematic review and meta-analysis. Immunopharmacol Immunotoxicol. 2014;36:251–260.
  • Hartman LLR, Crawford JR, Makale MT, et al. Pediatric phase II trials of poly-ICLC in the management of newly diagnosed and recurrent brain tumors. J Pediatr Hematol Oncol. 2014;36:451–457.
  • Jeung H-C, Moon YW, Rha SY, et al. Phase III trial of adjuvant 5-fluorouracil and adriamycin versus 5-fluorouracil, adriamycin, and polyadenylic-polyuridylic acid (poly A:U) for locally advanced gastric cancer after curative surgery: final results of 15-year follow-up. Ann Oncol Off J Eur Soc Med Oncol ESMO. 2008;19:520–526.
  • Kemeny N, Yagoda A, Wang Y, et al. Randomized trial of standard therapy with or without poly I:C in patients with superficial bladder cancer. Cancer. 1981;48:2154–2157.
  • Landolfo S, Guarini A, Riera L, et al. Chronic myeloid leukemia cells resistant to interferon-alpha lack STAT1 expression. Hematol J Off J Eur Haematol Assoc EHA. 2000;1:7–14.
  • Sun WH, Pabon C, Alsayed Y, et al. Interferon-alpha resistance in a cutaneous T-cell lymphoma cell line is associated with lack of STAT1 expression. Blood. 1998;91:570–576.
  • Krysko DV, Garg AD, Kaczmarek A, et al. Immunogenic cell death and DAMPs in cancer therapy. Nat Rev Cancer. 2012;12:860–875.
  • Schiavoni G, Sistigu A, Valentini M, et al. Cyclophosphamide synergizes with type I interferons through systemic dendritic cell reactivation and induction of immunogenic tumor apoptosis. Cancer Res. 2011;71:768–778.
  • Sistigu A, Yamazaki T, Vacchelli E, et al. Cancer cell-autonomous contribution of type I interferon signaling to the efficacy of chemotherapy. Nat Med. 2014;20:1301–1309.
  • Cooper ZA, Frederick DT, Juneja VR, et al. BRAF inhibition is associated with increased clonality in tumor-infiltrating lymphocytes. Oncoimmunology. 2013;2:e26615.

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